Zhenlong Zhou , Ruoxin Chen , Pengzhen Li , Penghui Fan , Lin Ma , Xinyu Cai , Yuchao Hou , Binbin Li , Jianyu Su
{"title":"Natural borneol improves cellular uptake of curcumin to enhance its photodynamic bactericidal activity against Escherichia coli ATCC 8739","authors":"Zhenlong Zhou , Ruoxin Chen , Pengzhen Li , Penghui Fan , Lin Ma , Xinyu Cai , Yuchao Hou , Binbin Li , Jianyu Su","doi":"10.1016/j.fm.2024.104686","DOIUrl":null,"url":null,"abstract":"<div><div>Photodynamic inactivation (PDI), a non-thermal sterilization method, has attracted considerable attention due to its broad-spectrum antimicrobial activity, environmental friendliness and cost-effectiveness. Curcumin (Cur), a food-grade photosensitizer, exhibits photodynamic antimicrobial activity based primarily on its efficiency in intracellular accumulation. However, Cur's low water solubility and the barriers presented by the outer membrane of Gram-negative bacteria challenge its ability to penetrate the cytoplasm. Natural borneol (NB), a monoterpene food flavoring agent, has also been shown to improve the efficiency of drug absorption. In this study, we demonstrated that NB significantly improved the cellular uptake of Cur, thereby enhancing its photodynamic bactericidal activity against Gram-negative <em>Escherichia coli</em> (<em>E. coli</em>) ATCC 8739, a potential alternative to enterohemorrhagic <em>E. coli</em> O157:H7. This effect was attributed to NB's ability to disrupt the integrity of the <em>E. coli</em> bacterial membrane, thereby increasing cellular permeability. Transcriptomic analysis further confirmed that NB dysregulated the expression of genes associated with bacterial membrane structure and function in <em>E. coli</em>. Consequently, the increased accumulation of Cur in <em>E. coli</em> led to excessive production of intracellular reactive oxygen species (ROS) upon exposure to 6.5 J/cm<sup>2</sup> blue light (BL). These ROS, analyzed biochemically and transcriptionally, primarily disrupted bacterial membrane structure and function, the antioxidant system, and ultimately caused bacterial death. Remarkably, this combined strategy not only reduced <em>E. coli</em> contamination in the tested orange juice, but also preserved its nutritional quality. In conclusion, this research provides an innovative and effective approach to maintaining food safety.</div></div>","PeriodicalId":12399,"journal":{"name":"Food microbiology","volume":"127 ","pages":"Article 104686"},"PeriodicalIF":4.5000,"publicationDate":"2024-11-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Food microbiology","FirstCategoryId":"97","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0740002024002247","RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Photodynamic inactivation (PDI), a non-thermal sterilization method, has attracted considerable attention due to its broad-spectrum antimicrobial activity, environmental friendliness and cost-effectiveness. Curcumin (Cur), a food-grade photosensitizer, exhibits photodynamic antimicrobial activity based primarily on its efficiency in intracellular accumulation. However, Cur's low water solubility and the barriers presented by the outer membrane of Gram-negative bacteria challenge its ability to penetrate the cytoplasm. Natural borneol (NB), a monoterpene food flavoring agent, has also been shown to improve the efficiency of drug absorption. In this study, we demonstrated that NB significantly improved the cellular uptake of Cur, thereby enhancing its photodynamic bactericidal activity against Gram-negative Escherichia coli (E. coli) ATCC 8739, a potential alternative to enterohemorrhagic E. coli O157:H7. This effect was attributed to NB's ability to disrupt the integrity of the E. coli bacterial membrane, thereby increasing cellular permeability. Transcriptomic analysis further confirmed that NB dysregulated the expression of genes associated with bacterial membrane structure and function in E. coli. Consequently, the increased accumulation of Cur in E. coli led to excessive production of intracellular reactive oxygen species (ROS) upon exposure to 6.5 J/cm2 blue light (BL). These ROS, analyzed biochemically and transcriptionally, primarily disrupted bacterial membrane structure and function, the antioxidant system, and ultimately caused bacterial death. Remarkably, this combined strategy not only reduced E. coli contamination in the tested orange juice, but also preserved its nutritional quality. In conclusion, this research provides an innovative and effective approach to maintaining food safety.
光动力灭活(PDI)是一种非热灭菌方法,因其广谱抗菌活性、环保性和成本效益而备受关注。姜黄素(Cur)是一种食品级光敏剂,其光动力抗菌活性主要基于其在细胞内积累的效率。然而,姜黄素的水溶性较低,而且革兰氏阴性细菌的外膜对其渗透细胞质的能力构成了挑战。天然龙脑(NB)是一种单萜类食品调味剂,也被证明可以提高药物吸收效率。在这项研究中,我们证实 NB 能显著提高 Cur 的细胞吸收率,从而增强其对革兰氏阴性大肠杆菌(E. coli)ATCC 8739(肠出血性大肠杆菌 O157:H7 的潜在替代物)的光动力杀菌活性。这种效应归因于 NB 能够破坏大肠杆菌细菌膜的完整性,从而增加细胞的通透性。转录组分析进一步证实,NB 使大肠杆菌中与细菌膜结构和功能相关的基因表达失调。因此,在暴露于 6.5 J/cm2 蓝光(BL)时,大肠杆菌中 Cur 的积累增加,导致细胞内活性氧(ROS)产生过多。通过生化和转录分析,这些 ROS 主要破坏了细菌的膜结构和功能以及抗氧化系统,并最终导致细菌死亡。值得注意的是,这种综合策略不仅减少了测试橙汁中的大肠杆菌污染,还保持了其营养品质。总之,这项研究为维护食品安全提供了一种创新而有效的方法。
期刊介绍:
Food Microbiology publishes original research articles, short communications, review papers, letters, news items and book reviews dealing with all aspects of the microbiology of foods. The editors aim to publish manuscripts of the highest quality which are both relevant and applicable to the broad field covered by the journal. Studies must be novel, have a clear connection to food microbiology, and be of general interest to the international community of food microbiologists. The editors make every effort to ensure rapid and fair reviews, resulting in timely publication of accepted manuscripts.